ABSTRACT
The coast of northern Chile has been sparsely studied in regards to its invertebrate
fauna, with just a few works reviewing the distribution of local mollusks. This work
presents a survey of the shallow water heterobranch sea slugs currently occurring
around the port of Caldera (27 S), in the Región de Atacama, northern Chile.
Eight species of sea slugs were found in this study: Aplysiopsis cf. brattstroemi
(Marcus, 1959), Baptodoris peruviana (d’Orbigny, 1837), Diaulula variolata
(d’Orbigny, 1837), Doris fontainii d’Orbigny, 1837, Onchidella marginata (Couthouy
in Gould, 1852), Phidiana lottini (Lesson, 1831), Tyrinna delicata (Abraham, 1877)
and the new species Berthella schroedli sp. nov., described herein. All of the species
found in the area are endemic to South America, having distributions in the
southeastern Pacific and South Atlantic Oceans, from Ancash, Perú to Peninsula
Valdés, Argentina, and two of them represent species which are endemic to the
Chilean coasts (Aplysiopsis cf. brattstroemi and Berthella schroedli). The finding
of a previously undescribed species emphasizes the need of further surveys,
particularly in subtidal and deeper waters, in order to improve the knowledge
on this neglected fauna in Atacama.
Submitted 10 November 2015
Accepted 2 April 2016
Published 2 May 2016 Subjects Biodiversity, Conservation Biology, Marine Biology, Taxonomy, Zoology
Keywords Eastern Pacific, New taxa, Nudibranchia, Opisthobranchia, Pleurobranchidae,
Corresponding author
Sacoglossa, Onchidiidae, Chromodorididae, Dorididae, Shallow water
Juan Francisco Araya,
jfaraya@u.uchile.cl
INTRODUCTION
Academic editor
Robert Toonen The mollusks of the Región de Atacama, in northern Chile, have been sparsely studied;
Additional Information and most of the species commonly present in the area were described in the nineteenth
Declarations can be found on century (Broderip & Sowerby, 1832; Sowerby, 1832; Sowerby, 1833; d’Orbigny, 1834–1847;
page 15 Gould, 1852; Hupé, 1854; Gay, 1854, Philippi, 1860, among others), with a few works
DOI 10.7717/peerj.1963 reviewing species during the past century (Dall, 1909; Gigoux, 1932; Gigoux, 1934; Rehder,
Copyright 1945) and, more recently, with several works describing new species (Osorio, 2012; Araya,
2016 Araya & Valdés
2013; Araya, 2015a; Araya, 2015b; Miquel & Araya, 2013; Collado, 2015; Araya & Reid,
Distributed under
2016) or giving new records (Araya & Araya, 2015a). Regarding heterobranch sea slugs
Creative Commons CC-BY 4.0
in particular (sensu Camacho-Garcı́a et al. (2014) and Padula, Wirtz & Schrödl (2014)),
How to cite this article Araya and Valdés (2016), Shallow water heterobranch sea slugs (Gastropoda: Heterobranchia) from the Región de
Atacama, northern Chile. PeerJ 4:e1963; DOI 10.7717/peerj.1963
Table 1 Heterobranch sea slugs found in the Region of Atacama, northern Chile; species, distribution, ecology and references. Occurring
species involve those cited by Marcus (1959), Schrödl (1996a), Schrödl (2003), and material examined in this work.
Species Distribution Ecology References
Aplysiopsis cf. brattstroemi Antofagasta (23 39′S; 70 25′W) to Bahia de Sea floor, subtidal Schrödl (1996a)
(Marcus, 1959) Coliumo (36 32′S; 72 57′W), Chile
Baptodoris peruviana San Lorenzo (12 S), Peru to Valparaiso, Sea floor, epifaunal, subtidal Fischer & Cervera (2005a) and Fischer &
(d’Orbigny, 1837) Chile (33 02′S, 71 38′W) Cervera (2005b)
Berthella schroedli sp. n. Caldera (27 S), Chile Under sunken rocks, infaunal, This work
subtidal
Diaulula variolata Ica (14 S), Perú to Bahı́a de San Vicente Sea floor, epifaunal, subdtidal Fischer & Cervera (2005a), Fischer &
(d’Orbigny, 1837) (36 S), Chile Cervera (2005b) and Uribe et al.
(2013)
Doris fontainii Islote Ferrol (09 08′22″S; 78 37′15″W), Sea floor, epifaunal, subtidal Uribe et al. (2013) and Valdés &
(d’Orbigny, 1837) Ancash, Peru to northern Argentina Muniaı́n (2002)
Onchidella marginata Iquique (20 S), Chile to Isla de los Estados Under rocks, epifaunal, Rosenfeld & Aldea (2010)
(Couthoy in Gould, 1852) (coordinates), Argentina intertidal
Phidiana lottini (Lesson, Callao (12 02′S), Peru to Comau Fjord Sea floor, epifaunal, subtidal Schrödl et al. (2005), Uribe et al. (2013)
1831) (42 15′S; 72 25′12′W), Chile and Schrödl & Hooker (2014)
Tyrinna delicata (Abraham, Isla Blanca (09 S), Ancash, Peru to Sea floor, epifaunal, subtidal Schrödl & Millen (2001) and Uribe et al.
1877) Peninsula Valdés, in the Atlantic Magellan (2013)
Strait
only the studies by Bergh (1898), Marcus (1959), Schrödl (1996a), Schrödl (1996b), Schrödl
(1997), Schrödl (2003), Fischer, van de Velde & Roubos (2007) and most recently Labrı́n,
Guzmán & Sielfeld (2015) have included species from northern Chile. However, a few
recent papers dealing with the Peruvian fauna, including some species commonly found
in Chilean waters (e.g., Millen et al., 1994; Nakamura, 2006; Nakamura, 2007; Martynov &
Schrödl, 2011; Uribe & Pacheco, 2012; Uribe et al., 2013; Schrödl & Hooker, 2014 and others)
have also contributed to the knowledge of this group in the southeastern Pacific.
The present study provides records of sea slugs found in shallow waters around Caldera
(27 S), Región de Atacama, northern Chile. The coast of this area consists of rocky
formations with sparse sandy beaches and a comparatively narrow intertidal zone. Rocky
platforms, boulder fields and intertidal pools are common; however, some sheltered
areas have open sandy beaches, usually exposed to strong surf. All of the species reviewed
in this work are endemic to southern South America; with two of them presenting
new distributional records in Chile (Table 1). The aim of this preliminary study is to
contribute to the knowledge of the molluscan fauna in Chile, particularly from the largely
neglected northern coasts.
RESULTS
Systematics
Heterobranchia
Order Nudibranchia Cuvier, 1817
Superfamily Aeolidioidea Gray, 1827
Family Facelinidae Bergh, 1889
Genus Phidiana Gray, 1850
Type species Eolidia patagonica d’Orbigny, 1836, by subsequent designation by Alder &
Hancock (1855).
Superfamily Doridoidea
Family Chromodorididae Bergh, 1891
Genus Tyrinna Bergh, 1898
Type species Tyrinna nobilis Bergh, 1898 (= Tyrinna delicata (Abraham, 1877)), by
monotypy.
Mantle lacking an anterior notch. Rhinophores short and stout, joined together at the
base. Foot bilabiate anteriorly. Oral veil trapezoidal, protruding from the mantle. Gill
located on the right side of the body, lying longitudinally between the mantle and the foot;
it is attached to the body for more than half of its length. Gill bipinnate, with 13 pinnae on
either side of the rachis. Rachis smooth, lacking tubercles. Anus located dorsal to the
central area of the gill. Egg masses are small white spiral ribbons, up to about 25 mm in
diameter (Fig. 6C).
Shell: Shell fully internal, flattened, rectangular/oval in shape, elongate and located
centrally in the dorsal area, where it covers completely the viscera. Shell reddish brown in
color, somewhat nacreous/iridescent, with radial rays of pale yellowish which are visible
through the mantle in living specimens. Margins of shell sharp and fragile. Protoconch of
about 300 mm in diameter, smooth under low magnification. Teleoconch with fine
concentric ridges crossed by very fine radial striae, the first whorls have a cancellated
sculpture (Fig. 3C). Radula: Radular formula: 50–53 45–56.0.45–56. Radular teeth
hook-shaped lacking denticles (Fig. 4A). Innermost lateral teeth slightly smaller than
those from the middle portion of the half row (Fig. 4B). Outermost lateral teeth with a
much more elongate cusp than the mid laterals (Fig. 4C). Jaws with elongate cruciform
elements rather slender, elongate and lanceolate with a narrower base; each element
consisting of a central cusp flanked by 2–3 denticles on either side of a prominent central
cusp (Fig. 4D). Reproductive system: The ampulla is long and muscular, merging
proximally into the female gland complex. The penis is wide, with an elongate tip; it
connects proximally into a short deferent duct that splits into the prostate and the
elongate, muscular penial gland. The prostate is convoluted and connects proximally
to the female gland complex. A small, unidentified glandular structure connects distally
into the prostate and is here referred to provisionally as prostatic gland (prg? in Fig. 5A).
The vagina is elongate, straight; it narrows and connects to the round and large bursa
copulatrix. The seminal receptacle is elongate, muscular and about twice as long as the
bursa copulatrix; it connects to the vagina before it enters the bursa copulatrix. A uterine
duct could not be observed (Fig. 5).
Habitat: This species is found exclusively under rocks sunken at low tide in an almost
infaunal habitat; it can be found associated to encrusting sponges, bryozoans, encrusting
algae and to communities of micromollusks including Acar pusilla (Sowerby, 1833),
Brachidontes granulata (Hanley, 1843), Liotia cancellata Gray, 1848 and Mitrella
unifasciata (Sowerby, 1832).
Distribution: This species is somewhat rare but broadly distributed in the area of
study; small populations were found only in four localities, in about 40 km of coast,
always under rocks. According to Schrödl (2003) this genus has records in southern, South
America from the southernmost Patagonian shelf (Burdwood Bank), southeastern
Atlantic Ocean to southern Chile and north to Quiriquina Island, central Chile. The genus
thus extends its distribution in Chile more than 1,100 km to the north.
Type species Onchidium nigricans Quoy & Gaimard, 1832, by subsequent designation
by Fischer and Crosse (1878).
DISCUSSION
The present work updates the knowledge on the scarcely known marine fauna of northern
Chile (in particular from the Región de Atacama); from the 65 species of sea slugs (only
including Nudibranchia and Pleurobranchoidea) recorded to live in Chilean waters
(Schrödl, 2003), eight species were recorded in the Región de Atacama, accounting for
about 12% of the Chilean sea slug fauna. All of the species occurring in the area have
widespread ranges in the southeastern Pacific Ocean, from Ancash, Peru to the Strait of
Magellan, in southern Chile and in the South Atlantic Ocean, to Peninsula Valdés, in
Argentina (Table 1). With the exception of Berthella schroedli sp. n., all of the species
found in the Región de Atacama also occur in central and southern Chile. The absence of
species previously cited for the area (Schrödl, 1996a; Schrödl, 2003; Schrödl & Hooker,
2014), for example Corambe lucea Marcus, 1959; Janolus rebeccae Schrödl, 1996a; Schrödl,
1996b; Okenia luna Millen et al., 1994 and Thecacera darwini Pruvot-Fol, 1950, among
others, could be explained due to the limit of sampling depth, which was restricted to the
lower intertidal areas with a maximum of 2 m depth.
Heterobranch sea slugs have been rarely treated in studies reviewing the biodiversity
of mollusks from northern Chile (e.g. Marincovich, 1973; Guzmán, Saá & Ortlieb, 1998),
despite the comparatively high number of species recorded in the country. This is in
part explained by the current lack of experts working actively in the field and the
ACKNOWLEDGEMENTS
We are very grateful to Marta Araya (Caldera, Chile) for her assistance in field
collecting, to Carlo Magenta Cunha (Academy of Natural Sciences of Drexel University,
Philadelphia, USA), and to Cecilia Osorio (Universidad de Chile, Santiago, Chile) for their
help with essential bibliography, to Dirk Schories (University of Rostock, Rostock,
Germany) for his help with the images and information on Berthella platei from southern
Chile and to Michael Schrödl (Zoologische Staatssammlung München, Germany) and two
anonymous reviewers for their helpful corrections and suggestions on the manuscript.
Funding
The authors received no funding for this work.
Competing Interests
The authors declare that they have no competing interests.
Author Contributions
Juan Francisco Araya conceived and designed the experiments, performed the
experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the
paper, prepared figures and/or tables, reviewed drafts of the paper.
Ángel Valdés conceived and designed the experiments, performed the experiments,
analyzed the data, contributed reagents/materials/analysis tools, wrote the paper,
prepared figures and/or tables, reviewed drafts of the paper.
Data Deposition
The following information was supplied regarding data availability:
The research in this article did not generate nor collect any raw data/code.
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